Skip to main content

Advertisement

SpringerLink
Log in

Endosymbiotic dinoflagellates pump iron: differences in iron and other trace metal needs among the Symbiodiniaceae

  • Report
  • Published:
Coral Reefs Aims and scope Submit manuscript

Abstract

Iron (Fe) is essential to the physiology and growth of marine phytoplankton. It remains unclear how important iron is to the functional ecology of symbiotic dinoflagellates in the family Symbiodiniaceae, and whether limitations in iron ultimately affect the health and productivity of coral hosts, especially during episodes of ocean warming. Five Symbiodiniaceae species (spanning three genera) were used to investigate the effects of reduced iron availability on cell growth and the acquisition of other trace metals. When grown under iron replete conditions, intracellular iron quotas (content) reflected a large biochemical demand and ranged from 7.8 to 23.1 mmol Fe mol Phosphorus−1. Symbiodinium necroappetens was the only species that acclimated and maintained high growth rates while subjected to the lowest iron treatment (250 pM Fe′). Cultures surviving under low iron concentrations experienced changes in cellular concentrations (and presumably their use as cofactors) of other trace metals (e.g., zinc, copper, cobalt, manganese, nickel, molybdenum, vanadium), in ways that were species-specific, and possibly related to the natural ecology of each species. These changes in trace metal contents may have cascading effects on vital biochemical functions such as metalloenzyme activities, photosynthetic performance, and macronutrient assimilation. Furthermore, these species-specific responses to iron limitation provide a basis for investigations on how iron availability effects cellular processes among species and genera of Symbiodiniaceae, and ultimately how metal shortages modulate the response of coral–algal mutualisms to physiological stressors.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Aichelman HE, Zimmerman RC, Barshis DJ (2019) Adaptive signatures in thermal performance of the temperate coral Astrangia poculata. The Journal of Experimental Biology 222:jeb189225

    PubMed  Google Scholar 

  • Anderson MA, Morel FMM (1982) The influence of aqueous iron chemistry on the uptake of iron by the coastal diatom Thalassiosira weissflogii. Limnology and Oceanography 27:789–813

    CAS  Google Scholar 

  • Aranda M, Li Y, Liew YJ, Baumgarten S, Simakov O, Wilson MC, Piel J, Ashoor H, Bougouffa S, Bajic VB, Ryu T, Ravasi T, Bayer T, Micklem G, Kim H, Bhak J, LaJeunesse TC, Voolstra CR (2016) Genomes of coral dinoflagellate symbionts highlight evolutionary adaptations conducive to a symbiotic lifestyle. Scientific Reports 6:39734

    CAS  PubMed  PubMed Central  Google Scholar 

  • Baker AC (2003) Flexibility and Specificity in Coral-Algal Symbiosis: Diversity, Ecology, and Biogeography of Symbiodinium. Annual Review of Ecology, Evolution, and Systematics 34:661–689

    Google Scholar 

  • Behrenfeld MJ, Milligan AJ (2013) Photophysiological expressions of iron stress in phytoplankton. Annual review of marine science 5:217–246

    PubMed  Google Scholar 

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society Series B (Methodological) 57:289–300

    Google Scholar 

  • Biscéré T, Ferrier-Pagès C, Gilbert A, Pichler T, Houlbrèque F (2018) Evidence for mitigation of coral bleaching by manganese. Scientific Reports 8:1–10

    Google Scholar 

  • Blaby-Haas CE, Merchant SS (2012) The ins and outs of algal metal transport. Biochimica et Biophysica Acta (BBA) - Molecular Cell Research 1823:1531–1552

    CAS  Google Scholar 

  • Brand LE, Sunda WG, Guillard RRL (1983) Limitation of marine phytoplankton reproductive rates by zinc, manganese, and iron. Limnology and Oceanography 28:1182–1198

    CAS  Google Scholar 

  • Crichton RR, Pierre JL (2001) Old iron, young copper: from Mars to Venus. Biometals 14:99–112

    CAS  PubMed  Google Scholar 

  • D’Angelo C, Wiedenmann J (2014) Impacts of nutrient enrichment on coral reefs: new perspectives and implications for coastal management and reef survival. Current Opinion in Environmental Sustainability 7:82–93

    Google Scholar 

  • Entsch B, Sim RG, Hatcher BG (1983) Indications from photosynthetic components that iron is a limiting nutrient in primary producers on coral reefs. Marine Biology 73:17–30

    CAS  Google Scholar 

  • Falkowski PG, Katz ME, Knoll AH, Quigg A, Raven JA, Schofield O, Taylor FJR (2004) The Evolution of Modern Eukaryotic Phytoplankton. Science 305:354

    CAS  PubMed  Google Scholar 

  • Ferrier-Pagès C, Sauzéat L, Balter V (2018) Coral bleaching is linked to the capacity of the animal host to supply essential metals to the symbionts. Global Change Biology 24:3145–3157

    PubMed  Google Scholar 

  • Goyen S, Pernice M, Szabó M, Warner ME, Ralph PJ, Suggett DJ (2017) A molecular physiology basis for functional diversity of hydrogen peroxide production amongst Symbiodinium spp. (Dinophyceae). Marine Biology 164:46

    Google Scholar 

  • Guillard RRL, Hargraves PE (1993) Stichochrysis immobilis is a diatom, not a chrysophyte. Phycologia 32:234–236

    Google Scholar 

  • Ho T-Y (2013) Nickel limitation of nitrogen fixation in Trichodesmium. Limnology and Oceanography 58:112–120

    CAS  Google Scholar 

  • Ho T-Y, Chien C-T, Wang B-N, Siriraks A (2010) Determination of trace metals in seawater by an automated flow injection ion chromatograph pretreatment system with ICPMS. Talanta 82:1478–1484

    CAS  PubMed  Google Scholar 

  • Ho T-Y, Quigg A, Finkel ZV, Milligan AJ, Wyman K, Falkowski PG, Morel FMM (2003) The Elemental composition of some marine phytoplankton. J Phycol 39:1145–1159

    CAS  Google Scholar 

  • Hoadley KD, Lewis AM, Wham DC, Pettay DT, Grasso C, Smith R, Kemp DW, LaJeunesse TC, Warner ME (2019) Host–symbiont combinations dictate the photo-physiological response of reef-building corals to thermal stress. Scientific Reports 9:9985

    PubMed  PubMed Central  Google Scholar 

  • Hoffmann LJ, Breitbarth E, Boyd PW, Hunter KA (2012) Influence of ocean warming and acidification on trace metal biogeochemistry. Mar Ecol Prog Ser 470:191–205

    CAS  Google Scholar 

  • Hopkinson BM, Morel FMM (2009) The role of siderophores in iron acquisition by photosynthetic marine microorganisms. BioMetals 22:659–669

    CAS  PubMed  Google Scholar 

  • Horwitz R, Borell EM, Fine M, Shaked Y (2014) Trace element profiles of the sea anemone Anemonia viridis living nearby a natural CO2 vent. PeerJ 2:e538

    PubMed  PubMed Central  Google Scholar 

  • Jeong HJ, Du Yoo Y, Kang NS, Lim AS, Seong KA, Lee SY, Lee MJ, Lee KH, Kim HS, Shin W (2012) Heterotrophic feeding as a newly identified survival strategy of the dinoflagellate Symbiodinium. Proceedings of the National Academy of Sciences 109:12604–12609

    CAS  Google Scholar 

  • Jeong HJ, Lee SY, Kang NS, Yoo YD, Lim AS, Lee MJ, Kim HS, Yih W, Yamashita H, LaJeunesse TC (2014) Genetics and morphology characterize the dinoflagellate Symbiodinium voratum, n. sp., (Dinophyceae) as the sole representative of Symbiodinium clade E. Journal of Eukaryotic Microbiology 61:75–94

    CAS  PubMed  Google Scholar 

  • Katz ME, Finkel ZV, Grzebyk D, Knoll AH, Falkowski PG (2004) Evolutionary Trajectories and Biogeochemical Impacts of Marine Eukaryotic Phytoplankton. Annual Review of Ecology, Evolution, and Systematics 35:523–556

    Google Scholar 

  • Kosman DJ (2003) Molecular mechanisms of iron uptake in fungi. Molecular Microbiology 47:1185–1197

    CAS  PubMed  Google Scholar 

  • Krueger T, Fisher PL, Becker S, Pontasch S, Dove S, Hoegh-Guldberg O, Leggat W, Davy SK (2015) Transcriptomic characterization of the enzymatic antioxidants FeSOD, MnSOD, APX and KatG in the dinoflagellate genus Symbiodinium. BMC Evolutionary Biology 15:1

    CAS  Google Scholar 

  • LaJeunesse TC (2005) “Species” radiations of symbiotic dinoflagellates in the Atlantic and Indo-Pacific since the Miocene-Pliocene transition. Molecular Biology and Evolution 22:570–581

    CAS  PubMed  Google Scholar 

  • LaJeunesse TC, Parkinson JE, Reimer JD (2012) A genetics-based description of Symbiodinium minutum sp. nov. and S. psygmophilum sp. nov. (Dinophyceae), two dinoflagellates symbiotic with cnidaria. Journal of Phycology 48:1380–1391

    PubMed  Google Scholar 

  • LaJeunesse TC, Lee SY, Gil-Agudelo DL, Knowlton N, Jeong HJ (2015) Symbiodinium necroappetens sp. nov. (Dinophyceae): an opportunist ‘zooxanthella’ found in bleached and diseased tissues of Caribbean reef corals. European Journal of Phycology 50:223–238

    Google Scholar 

  • LaJeunesse TC, Parkinson JE, Gabrielson PW, Jeong HJ, Reimer JD, Voolstra CR, Santos SR (2018) Systematic Revision of Symbiodiniaceae Highlights the Antiquity and Diversity of Coral Endosymbionts. Current Biology 28:2570–2580

    CAS  PubMed  Google Scholar 

  • Lesser MP (1996) Elevated temperatures and ultraviolet radiation cause oxidative stress and inhibit photosynthesis in symbiotic dinoflagellates. Limnology and Oceanography 41:271–283

    CAS  Google Scholar 

  • Levin RA, Beltran VH, Hill R, Kjelleberg S, McDougald D, Steinberg PD, van Oppen MJH (2016) Sex, scavengers, and chaperones: transcriptome secrets of divergent Symbiodinium thermal tolerances. Molecular Biology and Evolution: msw119

  • Lewis AM, Chan AN, LaJeunesse TC (2019) New Species of Closely Related Endosymbiotic Dinoflagellates in the Greater Caribbean have Niches Corresponding to Host Coral Phylogeny. Journal of Eukaryotic Microbiology 66:469–482

    PubMed  Google Scholar 

  • Liu X, Millero FJ (2002) The solubility of iron in seawater. Marine Chemistry 77:43–54

    CAS  Google Scholar 

  • Maldonado MT, Allen AE, Chong JS, Lin K, Leus D, Karpenko N, Harris SL (2006) Copper-dependent iron transport in coastal and oceanic diatoms. Limnology and Oceanography 51:1729–1743

    CAS  Google Scholar 

  • Mansour JS, Pollock FJ, Díaz-Almeyda E, Iglesias-Prieto R, Medina M (2018) Intra-and interspecific variation and phenotypic plasticity in thylakoid membrane properties across two Symbiodinium clades. Coral Reefs 37:841–850

    Google Scholar 

  • Martin JH, Gordon M, Fitzwater SE (1991) The case for iron. Limnology and Oceanography 36:1793–1802

    Google Scholar 

  • Martínez-Garcia A, Rosell-Melé A, Jaccard SL, Geibert W, Sigman DM, Haug GH (2011) Southern Ocean dust–climate coupling over the past four million years. Nature 476:312

    PubMed  Google Scholar 

  • Masmoudi S, Nguyen-Deroche N, Caruso A, Ayadi H, Morant-Manceau A, Tremblin G, Schoefs B (2013) Cadmium, copper, sodium and zinc effects on diatoms: From heaven to hell—A review. Cryptogamie, Algologie 34:185–225

    Google Scholar 

  • McGinty ES, Pieczonka J, Mydlarz LD (2012) Variations in Reactive Oxygen Release and Antioxidant Activity in Multiple Symbiodinium Types in Response to Elevated Temperature. Microb Ecol 64:1000–1007

    CAS  PubMed  Google Scholar 

  • Merchant SS (2007) Trace metal utilization in chloroplasts The structure and function of plastids. Springer, Berlin, pp 199–218

    Google Scholar 

  • Mitchelmore CL, Alan Verde E, Ringwood AH, Weis VM (2003) Differential accumulation of heavy metals in the sea anemone Anthopleura elegantissima as a function of symbiotic state. Aquatic Toxicology 64:317–329

    CAS  PubMed  Google Scholar 

  • Moore JK, Doney SC, Glover DM, Fung IY (2001) Iron cycling and nutrient-limitation patterns in surface waters of the World Ocean. Deep Sea Research Part II: Topical Studies in Oceanography 49:463–507

    Google Scholar 

  • Moore CM, Mills MM, Arrigo KR, Berman-Frank I, Bopp L, Boyd PW, Galbraith ED, Geider RJ, Guieu C, Jaccard SL, Jickells TD, La Roche J, Lenton TM, Mahowald NM, Maranon E, Marinov I, Moore JK, Nakatsuka T, Oschlies A, Saito MA, Thingstad TF, Tsuda A, Ulloa O (2013) Processes and patterns of oceanic nutrient limitation. Nature Geosci 6:701–710

    CAS  Google Scholar 

  • Morel FMM, Hudson RJM, Price NM (1991) Limitation of productivity by trace metals in the sea. Limnology and Oceanography 36:1742–1755

    CAS  Google Scholar 

  • Morel FMM, Rueter JG, Anderson DM, Guillard RRL (1979) Aquil: a chemically defined phytoplankton culture medium for trace metal studies. Journal of Phycology 15:135–141

    CAS  Google Scholar 

  • Morel FMM, Reinfelder JR, Roberts SB, Chamberlain CP, Lee JG, Yee D (1994) Zinc and carbon co-limitation of marine phytoplankton. Nature 369:740

    CAS  Google Scholar 

  • Muggli DL, Harrison PJ (1996) Effects of nitrogen source on the physiology and metal nutrition of Emiliania huxleyi grown under different iron and light conditions. Mar Ecol Prog Ser 130:255–267

    CAS  Google Scholar 

  • Parkinson JE, Banaszak AT, Altman NS, LaJeunesse TC, Baums IB (2015) Intraspecific diversity among partners drives functional variation in coral symbioses. Scientific Reports 5:15667

    CAS  PubMed  PubMed Central  Google Scholar 

  • Parkinson JE, Baumgarten S, Michell CT, Baums IB, LaJeunesse TC, Voolstra CR (2016) Gene expression variation resolves species and individual strains among coral-associated dinoflagellates within the genus Symbiodinium. Genome Biology and Evolution 8:665–680

    PubMed  PubMed Central  Google Scholar 

  • Pohlert T (2014) The pairwise multiple comparison of mean ranks package (PMCMR). R package: 2004–2006

  • Puig S, Andrés-Colás N, García-Molina A, Peñarrubia L (2007) Copper and iron homeostasis in Arabidopsis: responses to metal deficiencies, interactions and biotechnological applications. Plant, Cell & Environment 30:271–290

    CAS  Google Scholar 

  • Ragni M, Airs RL, Hennige SJ, Suggett DJ, Warner ME, Geider RJ (2010) PSII photoinhibition and photorepair in Symbiodinium (Pyrrhophyta) differs between thermally tolerant and sensitive phylotypes. Mar Ecol Prog Ser 406:57–70

    CAS  Google Scholar 

  • Raven JA (1988) The iron and molybdenum use efficiencies of plant growth with different energy, carbon and nitrogen sources. New Phytologist 109:279–287

    CAS  Google Scholar 

  • Raven JA, Evans MCW, Korb RE (1999) The role of trace metals in photosynthetic electron transport in O2-evolving organisms. Photosynthesis Research 60:111–150

    CAS  Google Scholar 

  • Redfield AC (1934) On the proportions of organic derivatives in sea water and their relation to the composition of plankton. James Johnstone Memorial Volume: 176–192

  • Reichelt-Brushett AJ, McOrist G (2003) Trace metals in the living and nonliving components of scleractinian corals. Marine Pollution Bulletin 46:1573–1582

    CAS  PubMed  Google Scholar 

  • Rodriguez IB, Ho T-Y (2017) Interactive effects of spectral quality and trace metal availability on the growth of Trichodesmium and Symbiodinium. PLOS ONE 12:e0188777

    PubMed  PubMed Central  Google Scholar 

  • Rodriguez IB, Ho T-Y (2018) Trace Metal Requirements and Interactions in Symbiodinium kawagutii. Frontiers in Microbiology 9:142

    PubMed  PubMed Central  Google Scholar 

  • Rodriguez IB, Lin S, Ho J, Ho T-Y (2016) Effects of Trace Metal Concentrations on the Growth of the Coral Endosymbiont Symbiodinium kawagutii. Frontiers in Microbiology 7:82

    PubMed  PubMed Central  Google Scholar 

  • Shaked Y, Xu Y, Leblanc K, Morel FMM (2006) Zinc availability and alkaline phosphatase activity in Emiliania huxleyi: Implications for Zn-P co-limitation in the ocean. Limnology and Oceanography 51:299–309

    CAS  Google Scholar 

  • Shick JM, Iglic K, Wells ML, Trick CG, Doyle J, Dunlap WC (2011) Responses to iron limitation in two colonies of Stylophora pistillata exposed to high temperature: Implications for coral bleaching. Limnology and Oceanography 56:813–828

    CAS  Google Scholar 

  • Shoguchi E, Shinzato C, Kawashima T, Gyoja F, Mungpakdee S, Koyanagi R, Takeuchi T, Hisata K, Tanaka M, Fujiwara M (2013) Draft assembly of the Symbiodinium minutum nuclear genome reveals dinoflagellate gene structure. Current Biology 23:1399–1408

    CAS  PubMed  Google Scholar 

  • Smalley GW, Coats WD, Stoecker DK (2003) Feeding in the mixotrophic dinoflagellate Ceratium furca is influenced by intracellular nutrient concentrations. Mar Ecol Prog Ser 262:137–151

    Google Scholar 

  • Soria-Dengg S, Horstmann U (1995) Ferrioxamines B and E as iron sources for the marine diatom Phaeodactylum tricornutum. Mar Ecol Prog Ser 127:269–277

    CAS  Google Scholar 

  • Stoecker DK, Li A, Coats DW, Gustafson DE, Nannen MK (1997) Mixotrophy in the dinoflagellate Prorocentrum minimum. Mar Ecol Prog Ser 152:1–12

    Google Scholar 

  • Stossel TP (1974) Phagocytosis. New England Journal of Medicine 290:774–780

    Google Scholar 

  • Strzepek RF, Harrison PJ (2004) Photosynthetic architecture differs in coastal and oceanic diatoms. Nature 431:689

    CAS  PubMed  Google Scholar 

  • Sunda WG, Huntsman SA (1995) Iron uptake and growth limitation in oceanic and coastal phytoplankton. Marine Chemistry 50:189–206

    CAS  Google Scholar 

  • Team RC (2016) R: A language and environment for statistical computing [Computer software]. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Thornhill DJ, Kemp DW, Bruns BU, Fitt WK, Schmidt GW (2008) Correspondence between cold tolerance and temperate biogeography in a Western Atlantic symbiodinium (Dinophyta) lineage 1. J Phycol 44(5):1126–1135

    CAS  PubMed  Google Scholar 

  • Twining BS, Baines SB (2013) The trace metal composition of marine phytoplankton. Annual Review of Marine Science 5:191–215

    PubMed  Google Scholar 

  • Wang B-S, Lee C-P, Ho T-Y (2014) Trace metal determination in natural waters by automated solid phase extraction system and ICP-MS: The influence of low level Mg and Ca. Talanta 128:337–344

    CAS  PubMed  Google Scholar 

  • Wickham H (2009) ggplot2: Elegant Graphics for Data Analysis. Springer, New York

    Google Scholar 

  • Wiedenmann J, D'Angelo C, Smith EG, Hunt AN, Legiret F-E, Postle AD, Achterberg EP (2013) Nutrient enrichment can increase the susceptibility of reef corals to bleaching. Nature Clim Change 3:160–164

    CAS  Google Scholar 

  • Wilhelm SW, Maxwell DP, Trick CG (1996) Growth, iron requirements, and siderophore production in iron-limited Synechococcus PCC 72. Limnology and Oceanography 41:89–97

    CAS  Google Scholar 

  • Wilke CO (2016) cowplot: Streamlined plot theme and plot annotations for ggplot2 [Software]

  • Wolfe-Simon F, Grzebyk D, Schofield O, Falkowski PG (2005) The role and evolution of superoxide dismutases in algae. Journal of Phycology 41:453–465

    CAS  Google Scholar 

  • Wood PM (1978) Interchangeable copper and iron proteins in algal photosynthesis. The FEBS Journal 87:9–19

    CAS  Google Scholar 

Download references

Acknowledgements

The authors thank Jie-Cheng Chang, Wan-Yen Cheng, and Wan-Chen Tu for technical support. This work was funded by NSF-EAPSI and MOST #1713926 (to HGR), NASA PA Space Grant Fellowship (to HGR), NSF-BIO-OCE #1636022 (to TCL), MOST 106-2611-M-001-003 (to TYH), MOST 107-2611-M-001-001 (to TYH), and Academia Sinica Career Development Award (to TYH). We are grateful to the two anonymous reviewers whose comments improved the quality of the paper.

Author information

Author notes

  1. Irene B. Rodriguez

    Present address: Marine Science Institute, University of the Philippines Diliman, Quezon City, Philippines

Authors and Affiliations

  1. Department of Biology, The Pennsylvania State University, University Park, PA, 16802, USA

    Hannah G. Reich & Todd C. LaJeunesse

  2. Research Center for Environmental Changes, Academia Sinica, Taipei, Taiwan

    Irene B. Rodriguez & Tung-Yuan Ho

  3. Institute of Oceanography, National Taiwan University, Taipei, Taiwan

    Tung-Yuan Ho

Authors
  1. Hannah G. Reich
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Irene B. Rodriguez
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Todd C. LaJeunesse
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Tung-Yuan Ho
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Hannah G. Reich or Tung-Yuan Ho.

Ethics declarations

Conflict of interest

On behalf of all authors, the co-corresponding authors state that there is no conflict of interest.

Additional information

Topic Editor Simon Davy

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Reich, H.G., Rodriguez, I.B., LaJeunesse, T.C. et al. Endosymbiotic dinoflagellates pump iron: differences in iron and other trace metal needs among the Symbiodiniaceae. Coral Reefs 39, 915–927 (2020). https://doi.org/10.1007/s00338-020-01911-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00338-020-01911-z

Keywords

Search

Navigation